Abstract
Gene expression evolution through gene regulatory network (GRN) changes has gained appreciation as a driver of morphological evolution. However, understanding how GRNs evolve is hampered by finding relevant cis-regulatory element (CRE) mutations, and interpreting the protein-DNA interactions they alter. We investigated evolutionary changes in the duplicated Bric-à-brac (Bab) transcription factors and a key Bab target gene in a GRN underlying the novel dimorphic pigmentation of D. melanogaster and its relatives. It has remained uncertain how Bab was integrated within the pigmentation GRN. Here, we show that the ancestral transcription factor activity of Bab gained a role in sculpting sex-specific pigmentation through the evolution of binding sites in a CRE of the pigment-promoting yellow gene. This work demonstrates how a new trait can evolve by incorporating existing transcription factors into a GRN through CRE evolution, an evolutionary path likely to predominate newly evolved functions of transcription factors.
Highlights
Transcription factors play central roles in the development and evolution of animal traits by binding to cis-regulatory elements to spatially- and temporally-regulate patterns of gene expression (Davidson, 2006; Levine, 2010)
These results suggest that the direct Bab regulation of yellow evolved within the dimorphic body element, coincident with the evolution of the dimorphic pigmentation trait. 372 373 Discussion Here, we investigated the functions and evolution of the paralogous D. melanogaster Bab1 and Bab2 proteins that perform a key regulatory role in a gene regulatory networks (GRN) controlling a male376 specific pigmentation trait. Though these two paralogs descend from an ancient duplication event (Figure 1A), our results show that their ability to function in D. melanogaster pigmentation required little-to-no alteration in the functional capability of the Bab proteins
Our data point to the evolution of binding sites in a cis-regulatory element (CRE) of a key pigmentation gene yellow to which these proteins bind through their DNA binding domains (Figure 8A)
Summary
Transcription factors play central roles in the development and evolution of animal traits by binding to cis-regulatory elements to spatially- and temporally-regulate patterns of gene expression (Davidson, 2006; Levine, 2010). As transcription factor genes are generally much older than the traits they impact, a central question of evolutionary developmental biology is the relative role that gene duplication, protein coding and CRE sequence evolution play in the evolution of GRNs for novel traits (Carroll, 2008; Stern and Orgogozo, 2008). Answers to this question require studies of recently evolved traits for which the derived and ancestral states of genes and gene components can be inferred through manipulative studies of GRN function (Rebeiz and Williams, 2011). One enzyme, encoded by the yellow gene is activated through a CRE known as the “body element” (Camino et al., 2015; Wittkopp et al, 2002) that possesses at least two binding sites for the Hox factor
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